Low anticoagulant heparin targets multiple sites of inflammation, suppresses heparin-induced thrombocytopenia, and inhibits interaction of RAGE with its ligands

Am J Physiol Cell Physiol. 2010 Jul;299(1):C97-110. doi: 10.1152/ajpcell.00009.2010. Epub 2010 Apr 7.

Abstract

While heparin has been used almost exclusively as a blood anticoagulant, important literature demonstrates that it also has broad anti-inflammatory activity. Herein, using low anti-coagulant 2-O,3-O-desulfated heparin (ODSH), we demonstrate that most of the anti-inflammatory pharmacology of heparin is unrelated to anticoagulant activity. ODSH has low affinity for anti-thrombin III, low anti-Xa, and anti-IIa anticoagulant activities and does not activate Hageman factor (factor XII). Unlike heparin, ODSH does not interact with heparin-platelet factor-4 antibodies present in patients with heparin-induced thrombocytopenia and even suppresses platelet activation in the presence of activating concentrations of heparin. Like heparin, ODSH inhibits complement activation, binding to the leukocyte adhesion molecule P-selectin, and the leukocyte cationic granular proteins azurocidin, human leukocyte elastase, and cathepsin G. In addition, ODSH and heparin disrupt Mac-1 (CD11b/CD18)-mediated leukocyte adhesion to the receptor for advanced glycation end products (RAGE) and inhibit ligation of RAGE by its many proinflammatory ligands, including the advanced glycation end-product carboxymethyl lysine-bovine serum albumin, the nuclear protein high mobility group box protein-1 (HMGB-1), and S100 calgranulins. In mice, ODSH is more effective than heparin in reducing selectin-mediated lung metastasis from melanoma and inhibits RAGE-mediated airway inflammation from intratracheal HMGB-1. In humans, 50% inhibitory concentrations of ODSH for these anti-inflammatory activities can be achieved in the blood without anticoagulation. These results demonstrate that the anticoagulant activity of heparin is distinct from its anti-inflammatory actions and indicate that 2-O and 3-O sulfate groups can be removed to reduce anticoagulant activity of heparin without impairing its anti-inflammatory pharmacology.

Publication types

  • Clinical Trial, Phase I
  • Randomized Controlled Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / administration & dosage
  • Anti-Inflammatory Agents / adverse effects
  • Anti-Inflammatory Agents / pharmacokinetics
  • Anti-Inflammatory Agents / pharmacology*
  • Anticoagulants / administration & dosage
  • Anticoagulants / adverse effects
  • Anticoagulants / pharmacokinetics
  • Anticoagulants / pharmacology*
  • Antithrombin III / metabolism
  • Blood Coagulation / drug effects*
  • Blood Coagulation Tests
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Factor XIIa / metabolism
  • Female
  • Glycation End Products, Advanced / metabolism
  • HMGB1 Protein / metabolism
  • Heparin / administration & dosage
  • Heparin / adverse effects
  • Heparin / analogs & derivatives*
  • Heparin / pharmacokinetics
  • Heparin / pharmacology
  • Humans
  • Infusions, Intravenous
  • Injections, Intravenous
  • Injections, Subcutaneous
  • Ligands
  • Lung Neoplasms / blood
  • Lung Neoplasms / prevention & control
  • Lung Neoplasms / secondary
  • Macrophage-1 Antigen / metabolism
  • Male
  • Melanoma, Experimental / blood
  • Melanoma, Experimental / drug therapy
  • Melanoma, Experimental / pathology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Nerve Growth Factors / metabolism
  • P-Selectin / metabolism
  • Platelet Activation / drug effects
  • Platelet Function Tests
  • Pneumonia / blood
  • Pneumonia / chemically induced
  • Pneumonia / drug therapy*
  • Receptor for Advanced Glycation End Products
  • Receptors, Immunologic / metabolism*
  • Recombinant Proteins / metabolism
  • S100 Calcium Binding Protein beta Subunit
  • S100 Proteins / metabolism
  • Thrombocytopenia / blood
  • Thrombocytopenia / chemically induced
  • Thrombocytopenia / prevention & control*
  • U937 Cells

Substances

  • Anti-Inflammatory Agents
  • Anticoagulants
  • Glycation End Products, Advanced
  • HMGB1 Protein
  • Ligands
  • Macrophage-1 Antigen
  • N-desulfated,2-O,3-O-desulfated heparin
  • Nerve Growth Factors
  • P-Selectin
  • Receptor for Advanced Glycation End Products
  • Receptors, Immunologic
  • Recombinant Proteins
  • S100 Calcium Binding Protein beta Subunit
  • S100 Proteins
  • Antithrombin III
  • Heparin
  • Factor XIIa